Bacteria As Biological Control Agents of Freshwater Cyanobacteria: Is It Feasible Beyond the Laboratory?
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Applied Microbiology and Biotechnology https://doi.org/10.1007/s00253-018-9391-9 MINI-REVIEW Bacteria as biological control agents of freshwater cyanobacteria: is it feasible beyond the laboratory? L. L. Ndlela1,2 & P. J. Oberholster1,2 & J. H. Van Wyk2 & P. H. Cheng1 Received: 27 July 2018 /Revised: 7 September 2018 /Accepted: 9 September 2018 # Springer-Verlag GmbH Germany, part of Springer Nature 2018 Abstract Biological control of cyanobacteria is a well-researched area with a central focus on laboratory-scale studies. Numerous reports have been made on algicidal isolates, with bacteria as a major component of the antagonists. The research in this review draws a brief summary of what is currently known in the area of freshwater cyanobacteria being inhibited by bacterial isolates. Proteobacteria, Bacteroidetes and Firmicutes are among the most commonly reported phyla of bacteria associated with or employed in this research area. However, there are limited reports of upscaling these control measures beyond the laboratory scale. Lytic control agents are the most commonly reported in the literature with subsequent cyanotoxin release. From a water quality perspective, this is not feasible. Based on the available literature, temperature, pH and nutrient changes have been explored in this short review as possible contributors to less optimal bacterial performance. Moreover, the investigation into optimising some of these parameters may lead to increased bacterial performance and, therefore, viability for upscaling this biological control. Through the compilation of current research, this review offers insight to live predator-prey cell interactions between cyanobacteria and algicidal bacteria. Keywords Algicidal bacteria . Cyanobacterial inhibition . Biological control . Harmful algal blooms Introduction they pose a threat to human and animal health, but they also present a challenge in terms of water treatment facilities The current research will assess the feasibility of bacteria as (Ndlela et al. 2016). A review by Paerl et al. (2016) has indi- cyanobacterial control agents beyond the laboratory. This will cated the significance in developing mitigation measures for be based on consolidation of the existing information on bio- cyanobacterial blooms, especially since they will be more dif- logical control of cyanobacteria, based on the reviews of Sigee ficult to curb due to increased temperatures caused by climate et al. (1999) and Gumbo et al. (2008)aswellasnumerous change in the future (Paerl et al. 2016). other publications on this topic. The focus will be more spe- The concept of biological control is the use of natural en- cifically in the area of bacteria as a biological control agent to emies to control a target organism, and among the measures living cyanobacterial cells in freshwater environments (Sigee previously mentioned in a review by Sigee et al. (1999), is the et al. 1999; Gumbo et al. 2008). use of bacteria as a means to control cyanobacterial cells. In With the rise in cyanobacterial bloom occurrences and tox- the broader focus of biological control, a review by icity, their mitigation is a crucial area of research. Lakes from Verschuere et al. (2000) thoroughly investigated the use of across the continents in the first world and developing coun- probiotic bacteria as possible biological control agents. The tries alike have been plagued with these blooms. Not only do key modes of action listed by bacteria as methods of biolog- ical control indicate antagonism as the more common mode of action in aquaculture (Verschuere et al. 2000). * L. L. Ndlela In the study of bacteria as control agents in aquaculture, a [email protected] variety of inhibitory compounds such as antibiotics, bacterio- cins, siderophores and lysosomes is produced by probiotic 1 Council for Scientific and Industrial Research, 11 Jan Celliers Road, bacteria. Whilst controlling other organisms, these com- Stellenbosch 7600, South Africa pounds can have a positive growth effect as well on unicellular 2 Department of Botany and Zoology, Faculty of Science, Stellenbosch algae and this needs to be clearly understood prior to University, Matieland 7600, South Africa Appl Microbiol Biotechnol implementation of certain species as biological control agents Control agents associated with cyanobacteria (Verschuere et al. 2000). and the susceptibility of the target Previous studies employing the use of bacteria in curbing microorganisms cyanobacteria have been conducted primarily at laboratory scale, with focus on a dominant species within a bloom or An extensive review (Van Wichelen et al. 2016) describes the on axenic cultures of a given cyanobacterial isolate susceptibility of Microcystis sp. to a variety of control agent (Nakamura et al. 2003; Choi et al. 2005; Jung et al. 2008; ranging from viruses to fungi and bacteria. The lack of appli- Shao et al. 2014;Suetal.2016a). These studies seldom ac- cation of this form of biological control outside laboratory count for the mixed cultures of phytoplankton or the possible conditions is also mentioned. This is of concern as a number variations in temperature during the exposures under lab con- of possible control measures with living organisms have been ditions or the fluctuations within the natural environment. A explored with minimal upscaling opportunities, with recom- recent study has found some of the interventions in curbing mendations made against upscaling beyond the lab in some cyanobacterial blooms were not as effective as reported, with studies (Kim et al. 2008). a strong caution to critically evaluate these control measures The first challenge comes from the lack of information on among which bacteria, artificial mixing and algae were men- the type of bacteria and interactions among species that may tioned (Lürling et al. 2016). hinder how effective a given control agent may be under field Recent research by Demeke (2016) describes the use of conditions as opposed to laboratory-based findings. The di- metabolites from the bacteria Flexibacterium in the control versity and intercellular interactions are numerous to be ade- of the filamentous cyanobacteria Oscillatoria and the lytic quately accounted for. To quantify or individually explore activity of the bacteria Bacillus against the cyanobacteria these factors is complex and requires further intensive re- Aphanizomenon flos-aquae (Demeke 2016). These are just a search to paint a more conclusive picture. Therefore, although few of many examples and show the interest and potential in there are numerous studies and reports of effective microor- the area of biological control. Over the past decade, advance- ganisms applicable in laboratory studies (Choi et al. 2005; ments in the use of bacteria as cyanobacterial control agents Jung et al. 2008; Kim et al. 2008; Zhang et al. 2016), none are not as extensive. of these have been conclusively upscaled or pursued beyond the lab due to the myriad of uncertainties that present them- selves within a mixed population. Another question that arises Aim of research is how well do these control agents regulate their algicidal characteristics in the natural environment within a mixed mi- crobial population? Taking a closer look at Microcystis spe- Although not exhaustive, this research aims to establish a cifically which has the most available literature and is the timeline of developments in this mode of cyanobacterial con- causative agent of the most common toxic blooms, if trol and what is currently known, with the intention of collat- cyanobacteria, particularly Microcystis, present such a wide ing pitfalls and possible future research challenges. The study susceptibility to environmental isolates, how they are able to is focused on the viability of this biological control and which continue proliferating and creating toxic aquatic conditions? factors could be optimised for further progress, based on the Table 1 presents a synopsis of the known types of control available literature. agents and the type of cyanobacterium they have a predatory or lytic impact on, exclusive of bacterial isolates from various studies (Zhang et al. 2008;Wangetal.2011; Gao et al. 2012a; Data collection approach Mialet et al. 2013; Mohamed et al. 2014; Leitão et al. 2018). The use of bacteria as control agents will be discussed in more The literature used within this mini-review was collected from depth in this review. the following databases: Google Scholar, Scopus and Another area of interest is the form of species, such as EBSCOhost with the following key words: Balgicidal Microcystis, as laboratory strains and their natural form. bacteria^, BMicrocystis/Oscillatoria/Cylindrospermopsis/ Generally, under natural conditions, these cells present as Anabaena/Aphanizomenon inhibiting bacteria^, Bbiological large colonial isolates with mucilage layers, surrounded by control of cyanobacteria^, Balgicidal bacteria^ and Bbacteria various microorganisms, which have been believed to have lysing cyanobacteria^, with the time frame delineated to symbiotic relations with the cyanobacteria. This colonial form 2000–2017. Further delineation was done based on focusing is not often observed in laboratory strains that present as uni- on freshwater-related studies and the lysis/suppression/control cellular, and a recent study (Geng et al. 2013) found that of living cyanobacterial cells by living bacterial agents, with laboratory-grown strains are not able to revert back to colonial minimal focus on microcystin degraders and bacterial metab-